Biological Invasions and Animal Behaviour.”

Aquatic Invasions (2019) Volume 14 Article in press Special Issue: Behaviour in Aquatic Invasions Guest editors: Kit Magellan, Amy Deacon, Marian Wong and Mhairi Alexander CORRECTED PROOF Book Review Highlights and Insights from “Biological Invasions and Animal Behaviour.” Daniel Sol1 and Judith S. Weis2,* 1CREAF Centre for Ecological Research and Forestry Applications, Barcelona, Catalonia, Spain 2Department of Biological Sciences, Rutgers University, Newark, NJ 07102, USA E-mail: [email protected] (DS), [email protected] (JSW) *Corresponding author Co-Editors’ Note: This paper is a contri- bution to the Behaviour in Aquatic Abstract Invasions Special Issue of Aquatic Invasions. Papers in this Special Issue Although behavior has long been considered central in understanding the causes and explore how behaviour contributes to consequences of animal invasions, “Biological Invasions and Animal Behaviour” invasion success; native species’ represents the first attempt to summarize the major advances in a single book. The behavioural strategies that reduce the book is a clear demonstration that behavior influences almost all facets of the impacts of invasions; how knowledge of behaviour can enhance management invasion process. However, a common theme of the book is that general rules are of invasive species; and potential effects rare. The role of behavior changes through the stages of the invasion process and of climate change on the behavioural within each stage can be highly context-dependent, implying that there may be impacts of aquatic invasive species. several ways of being a successful invader. Despite the scarcity of general rules, Citation: Sol D, Weis JS (2019) Highlights there are two recurring generalization that emerge from the book. One is the central and Insights from “Biological Invasions importance of behavioral plasticity in facilitating establishment and spread. The and Animal Behaviour.” Aquatic Invasions other is the appreciation that behavior is part of a suite of traits closely linked to life 14 (in press) history, whose effects on population dynamics vary as a function of population size Received: 2 October 2018 and degree of adaptive mismatch. Although aquatic ecologists have largely Accepted: 8 February 2019 contributed to developing these ideas, their research has often been restricted to a Published: 24 May 2019 few study systems and has mostly neglected mechanisms. Aquatic ecologists have, however, led research on the impact of invaders, using invasions as “unintended” Handling editor: Mhairi Alexander experiments for examining the consequences of novel species interactions. This Copyright: © Sol and Weis research unambiguously demonstrates that behavior is central to understanding how This is an open access article distributed under terms invaders alter native communities, notably by shaping predator–prey interactions. of the Creative Commons Attribution License (Attribution 4.0 International - CC BY 4.0). We believe that aquatic animals can continue providing research opportunities to further improve our understanding of the role of behavior in biological invasions, OPEN ACCESS. and we hope that “Biological Invasions and Animal Behaviour” may serve to encourage new research avenues. Key words: behavioral syndromes, plasticity, learning, foraging, dispersal, boldness, predator/prey interactions Behavior—the motor response to sensory information—has long been considered essential for understanding why some species succeed in new environments and what impacts they will have once established (Suarez and Cassey 2016). In the classic volume “Genetics of Colonizing Species,” Ernst Mayr (1965) highlighted the importance of behavior in defining the nature of successful invaders. For Mayr, behaviors such as the tendency to discover unoccupied habitats and the ability to shift habitat preferences were defining features of invasive species. Over 40 years later, researchers Sol and Weis (2019), Aquatic Invasions (in press) Highlights from Invasion Book have not only confirmed Mayr’s speculations on the central importance of behavior in invasions but have also found that the role of behavior is pervasive in almost all facets of biological invasions. The role of behavior in animal invasions is more complex than previously thought, however. For example, we now know that the behaviors that help negotiate particular stages of the invasion process (Figure 1) may have little impact, or even be detrimental, at other stages (Chapple and Wong 2016). Our edited book “Biological Invasions and Animal Behaviour”, published in 2016 by Cambridge University Press, summarizes the major advances. It contains contributions from researchers throughout the world who study the role of behavior in the invasion process from a variety of perspectives, approaches and study systems. Here, we summarize the most relevant contributions from the perspective of aquatic animals. Specifically, we discuss four major themes: 1) how the plastic nature of behavior assists individuals to thrive in novel environments, 2) how variation across individuals in less plastic behavior may also contribute to establishment by increasing the chances that some individuals are suitable to deal with the novel challenges and by facilitating evolutionary adjustments, 3) whether behavior should be considered as part of a life history syndrome to cope with environmental changes, and 4) how behavior helps predict the impact of biological invasions. The importance of behavioral plasticity to thrive in novel environments Novel environments confront animals with a wide variety of challenges, such as the need to adopt new foods or to avoid unfamiliar enemies. As behavior is an important way in which animals interact with their environment, the likelihood of establishment is expected to largely depend on the ability of individuals to adjust behavior to the new conditions. One way to do so is through decision-making. By choosing resources and habitats that better suit their phenotype, animals may enhance their fitness in novel environments (Sol and Maspons 2016; Sol et al. 2013). While aquatic ecologists have fundamentally contributed to our current understanding of the causes and consequences of such “Environmental matching choice”, the importance of this process in biological invasions has been under- appreciated. Instead, the importance of broad habitat and resource tolerances has attracted more interest, perhaps because many introduced animals are ecological generalists. In chapter 16, Tricarico and Acquiloni (2016) describe how alien crayfish occupy diverse habitats and tolerate a wide range of environmental conditions, features that are crucial for actively spreading to new habitats. Crayfish are omnivorous and opportunistic feeders, consuming a wide range of food items such as macrophytes, live macroinvertebrates, fish carrion, periphyton, detritus, Sol and Weis (2019), Aquatic Invasions (in press) Highlights from Invasion Book Figure 1. Stages of invasion and corresponding behavioural traits in the guppy. From Deacon and Magurran (2016) courtesy of Cambridge University Press. molted conspecifics, small live fish and tadpoles (Gherardi 2007). The red swamp crayfish Procambarus clarkii (Girard, 1852) for example, feeds on the diverse items in an invaded habitat in proportion to their availability so that its diet can change with habitats. Sol and Weis (2019), Aquatic Invasions (in press) Highlights from Invasion Book Although environmental matching choice should generally improve fitness in novel environments, it may also lead animals to prefer to settle in poor-quality habitats if the choice reflects the expression of a prewired genetic program and the cues used to make decisions have changed in the new environment. The existence of such ecological traps has been documented in sea turtles. Their hatchlings rely on light cues from the open horizon to orient after emerging, but light pollution from beachfront structures may lead them to migrate inland instead of towards the ocean (Witherington 1997). The existence of ecological traps highlights that even though the expression of innate behavioral responses provides certain plasticity to cope with environmental changes, it may not be enough to cope with many of the challenges of novel environments. However, animals can respond to novel challenges in yet another way, through learning. In a novel environment, animals need to learn things such as which foods are edible and safe, which habitats are safe and appropriate for their needs, where good breeding sites are located or which species are predators and how to avoid them (Griffin et al. 2016; Sol and Maspons 2016; Sol et al. 2005). Crayfish quickly learn to feed on unknown prey: in the laboratory, naive individuals of Procambarus clarkii require less than 12 hrs to learn to maximize capture rate of unfamiliar larvae (Ramalho and Anastacio 2011). Learning may thus facilitate establishment in novel environments by reducing environmental uncertainties and adaptive mismatches between the phenotype and the environment (Sol and Maspons 2016). Once acquired, novel learned behaviors may be rapidly transmitted to other individuals through social learning (Griffin et al. 2016; Sol and Maspons 2016). Focusing on guppies, Poecilia reticulata, Deacon and Magurran (2016) show how behavioral flexibility resulting from both individual innovation and social learning contributes to the invasion success of this species (Figure 1). As an omnivore, the guppy has dietary flexibility

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